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Ovariectomy predisposes female rats to fine particulate matter exposure’s effects by altering metabolic, oxidative, pro-inflammatory, and heat-shock protein levels

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Abstract

The reduction of estrogen levels, as a result of menopause, is associated with the development of metabolic diseases caused by alterations in oxidative stress (OS), inflammatory biomarkers, and 70-kDa heat-shock protein (HSP70) expression. Additionally, exposure to fine particulate matter air pollution modifies liver OS levels and predisposes organisms to metabolic diseases, such as type 2 diabetes (T2DM). We investigated whether ovariectomy affects hepatic tissue and alters glucose metabolism in female rats exposed to particulate air pollution. First, 24 female Wistar rats received an intranasal instillation of saline or particles suspended in saline 5 times per week for 12 weeks. The animals then received either bilateral ovariectomy (OVX) or false surgery (sham) and continued to receive saline or particles for 12 additional weeks, comprising four groups: CTRL, Polluted, OVX, and Polluted+OVX. Ovariectomy increased body weight and adiposity and promoted edema in hepatic tissue, hypercholesterolemia, glucose intolerance, and a pro-inflammatory profile (reduced IL-10 levels and increased IL-6/IL-10 ratio levels), independent of particle exposure. The Polluted+OVX group showed an increase in neutrophils and neutrophil/lymphocyte ratios, decreased antioxidant defense (SOD activity), and increased liver iHSP70 levels. In conclusion, alterations in the reproductive system predispose female organisms to particulate matter air pollution effects by affecting metabolic, oxidative, pro-inflammatory, and heat-shock protein expression.

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The data used to support the findings of this study are available from the corresponding authors upon request.

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Acknowledgments

The authors would like to thank colleagues from the Laboratory of Atmospheric Pollution (UFCSPA), all students from the Research Group in Physiology (UNIJUI), and Prof. Paulo Ivo Homem de Bittencourt Jr. from the Laboratory of Cellular Physiology (UFRGS) for their technical support.

Funding

This work was financially supported by the Regional University of Northwestern Rio Grande do Sul State (UNIJUI) and Federal University of Health Sciences of Porto Alegre (UFCSPA), as well as by grants from the Research Support Foundation of the State of Rio Grande do Sul (#ARD/PPP/FAPERGS/CNPq 08/2014, process 16/2551-0000196-0 to TGH) and the Brazilian National Council for Scientific and Technological Development (CNPq) (#MCTI/CNPq N° 01/2016 – CNPq, process 407329/2016-1 to TGH). LCCB was the recipient of a scholarship from the Coordination for the Improvement of Higher Education Personnel (CAPES), and JBS, LMS, and PTS were the recipients of a scholarship from FAPERGS and CNPq.

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  1. Research Group in Physiology, Department of Life Sciences, Regional University of Northwestern Rio Grande do Sul State (UNIJUÍ), Rua do Comércio, 3000 – Bairro Universitário, Ijuí, RS, 98700-000, Brazil

    Pauline Brendler Goettems-Fiorin, Lilian Corrêa Costa-Beber, Jaíne Borges dos Santos, Paula Taís Friske, Lucas Machado Sulzbacher, Matias Nunes Frizzo, Mirna Stela Ludwig & Thiago Gomes Heck

  2. Atmospheric Pollution Laboratory, Postgraduate Program in Health Sciences, Federal University of Health Sciences of Porto Alegre (UFCSPA), Rua Sarmento Leite, 245, Porto Alegre, RS, Brazil

    Pauline Brendler Goettems-Fiorin & Cláudia Ramos Rhoden

  3. Postgraduate Program in Integral Attention to Health (PPGAIS-UNIJUÍ/UNICRUZ), Ijuí, RS, Brazil

    Lilian Corrêa Costa-Beber, Matias Nunes Frizzo, Mirna Stela Ludwig & Thiago Gomes Heck

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  1. Pauline Brendler Goettems-Fiorin
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Contributions

PBGF completed all the experiments described in this manuscript. LCCB, JBS, PTF, and LMS performed the biometric and metabolic profile procedures and performed the administration of particles in the rats used in this study. LCCB, JBS, and LMS performed the experiments on oxidative stress parameters. JBS and LMS performed the Western blot analyses. MNF performed the hematological procedures. TGH performed eHSP70, cytokine, and eHSP70/iHSP70 ratio procedures. All authors were involved in analyzing the results. TGH and PBGF co-wrote the manuscript. Figure 1 was designed by TGH and PBGF. TGH, MSL, and CRR designed the study and provided experimental advice and helped with manuscript revision. All the authors had final approval of the submitted and published versions.

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Correspondence to Pauline Brendler Goettems-Fiorin or Thiago Gomes Heck.

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Goettems-Fiorin, P.B., Costa-Beber, L.C., dos Santos, J.B. et al. Ovariectomy predisposes female rats to fine particulate matter exposure’s effects by altering metabolic, oxidative, pro-inflammatory, and heat-shock protein levels. Environ Sci Pollut Res 26, 20581–20594 (2019). https://doi.org/10.1007/s11356-019-05383-9

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